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Turkish Journal of Zoology Turk J Zool (2017) 41: 329-334 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Short Communication doi:10.3906/zoo-1510-46

The blood sucking lice (Phthiraptera: Anoplura) of Croatia: review and new data

1, 2 Stjepan KRČMAR *, Tomi TRILAR 1 Department of Biology, J.J. Strossmayer University of Osijek, Osijek, Croatia 2 Slovenian Museum of Natural History, Ljubljana, Slovenia

Received: 17.10.2015 Accepted/Published Online: 24.06.2016 Final Version: 04.04.2017

Abstract: The present faunistic study of blood sucking lice (Phthiraptera: Anoplura) has resulted in the recording of the 4 : Hoplopleura acanthopus (Burmeister, 1839); Ho. affinis (Burmeister, 1839); Polyplax serrata (Burmeister, 1839), and apri Goureau, 1866 newly reported for the fauna of Croatia. Thirteen species and 2 subspecies are currently known from Croatia, belonging to 6 families. and Haematopinidae are the best represented families, with four species each, followed by and with two species each, Pediculidae with two subspecies, and Pthiridae with one species. Blood sucking lice were collected from 18 different host species. Three taxa, one species, and two subspecies were recorded on the Homo sapiens Linnaeus, 1758. Two species were recorded on Apodemus agrarius (Pallas, 1771); A. sylvaticus (Linnaeus, 1758); Bos taurus Linnaeus, 1758; and Sus scrofa Linnaeus, 1758 per host species. On the remaining 13 host species, one Anoplura species was collected. The recorded species were collected from 17 localities covering 17 fields of 10 × 10 km on the UTM grid of Croatia.

Key words: Phthiraptera, Anoplura, Croatia, species list

Phthiraptera have no free-living stage and represent Lice (Ferris, 1923). Ten years later, the first research of the the only order in which all species are known to be fauna of ectoparasites on domestic in Croatia permanent obligate ectoparasites of and in was carried out at the Department of Parasitology of the all developmental stages (Lyal, 1985; Mey, 2003; İnci et al., Veterinary Faculty in Zagreb (Babić, 1934). In that study 2010). This order comprises about 5000 species classified 22 species of Acari and 52 species of were recorded, in the following suborders: Anoplura, , of which seven species belong to blood sucking lice (Babić, , and Rhyncophthirina (İnci et al., 2010; Kenis 1934). From 5 October 1936 to 5 November 1937 studies and Roques, 2010). Adults range in length from less than of 50 sheep were carried out at the same faculty in order 0.5 to 11 mm, and have diversified into a great variety to determine the fauna of endoparasites. In that study one of morphological types (İnci et al., 2010). The blood species of blood sucking lice was recorded (Mikačić, 1938). sucking lice (Anoplura) are one of the smallest suborders Moreover, in a study of parasite fauna of cattle in the period of the order Phthiraptera, with more than 540 described from 11 October 1937 to 29 July 1940, two species of blood species (Light et al., 2010). They are ectoparasites of sucking lice were recorded (Mikačić, 1941). All together eutherian mammals, parasitizing members of 12 of the 29 eight species of blood sucking lice were collected in recognized mammalian orders and approximately 20% of Croatia in the period from 1934 to 1940. Some specimens all mammalian species (Durden and Musser, 1994; Reed et of blood sucking lice (Anoplura) were collected from the al., 2007; Hornok et al., 2010; Light et al., 2010). Sucking 1960s to the 1980s during studies of the ectoparasitical lice have great veterinary significance; firstly they cause entomofauna of Yugoslav mammals. In that research Savo economic loss in livestock production and secondly some Brelih and coworkers mainly presented the distribution species can transmit -borne pathogens to the hosts and taxonomic characteristic of (Siphonaptera) and (Hornok et al., 2010). This explains why they are the best chewing lice (Amblycera and Ischnocera), while blood studied suborder of the order Phthiraptera (Smith, 2003). sucking lice remained unpublished. Recently, in 2012 and Unfortunately, data on the fauna of blood sucking lice in 2014, some species of blood sucking lice were collected in Croatia are very scarce. The earliest data about the fauna eastern Croatia; thus the principal aim of the present study of blood sucking lice from Croatia appeared during the was to summarize all available data on the blood sucking 1920s in Contributions toward a Monograph of the Sucking lice fauna of Croatia. * Correspondence: [email protected] 329 KRČMAR and TRILAR / Turk J Zool

The sampling sites are listed numerically on the map in of rodent in central and eastern Croatia. The third new the Figure and UTM 10 × 10 km grid coordinates are given record P. serrata was collected in the lowlands, mountains, in the third column of the Table. The exact geographical and Mediterranean part of Croatia on four different rodent coordinates of sampling sites are given in the second hosts, while the fourth new record, Hae. apri, was collected column of the Table and were determined using Google from Mount Velebit on wild boar. Most of the species are Earth. The map was created by GPS Visualizer (Schneider, cosmopolitan (n = 9), (Durden and Musser, 1994). These 2003–2015). Most of the studied specimens are deposited species are pedalis (Osborn, 1896), L. setosus in the collections of the Slovenian Museum of Natural (von Olfers, 1816), L. stenopsis (Burmeister, 1838), L. vituli History (PMSL) in Ljubljana and in the Department of (Linnaeus, 1758), P. spinu l o s a , (Burmeister, 1839), Biology, JJ Strossmayer University of Osijek. Identification pubis (Linnaeus, 1758), Hae. asini (Linnaeus, 1758), Hae. was carried out using standard keys for Anoplura suis (Linnaeus, 1758), and humanus Linnaeus, (Toulechkoff, 1954; Piotrowski, 1970). The nomenclature 1758. The Eurasian endemic fauna is represented by the of Anoplura species and hosts follows the Fauna Europaea following species: Ho. affinis, P. serrata, and Hae. apri. Ho. database (de Jong, 2014) and integrated taxonomic acanthopus belongs to a Holarctic group of species, while information system for livestock (http://www.itis.usda. Hae. eurysternus (Nitzsch, 1818) is mainly distributed gov/). Six species of blood sucking lice were collected worldwide in temperate zones. In the first article about from domestic animals, as well as six species from wild ectoparasites on domestic animals in Croatia, Babić (1934) animals and two species from humans. From the material used the names L. piliferus (Burmeister), Enderlein 1904, examined, four species of Anoplura are new to the fauna and Hae. spinulosus Burmeister, which have become junior of Croatia. These areHoplopleura acanthopus, Ho. affinis, synonyms for L. setosus and P. spinu l os a . During the 1950s Polyplax serrata, and Haematopinus apri. Ho. acanthopus in Croatia, most studies on parasitic lice focused on chewing was collected in mountainous regions of Croatia on four lice fauna from the suborders Amblycera and Ischnocera different rodents. Ho. affinis was collected from one species (Vražić, 1956, 1957). Furthermore, during the second

Figure. Sampling sites of blood sucking lice (Phthiraptera: Anoplura) in Croatia.

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Table. List of sampling sites.

Locality Altitude-latitude (degree/min/sec) UTM 1. Vuka 45°26ʹ21ʺN, 18°30ʹ23ʺE CR 03 2. Bilje 45°36ʹ16ʺN, 18°44ʹ39ʺE CR 25 3. Otok 45°08ʹ47ʺN, 18°53ʹ01ʺE CR 30 4. Zmajevac 45°47ʹ59ʺN, 18°48ʹ23ʺE CR 37 5. Velika Kapela, Vrelo 45°13ʹ34ʺN, 14°56ʹ 55ʺE WL 00 6. Domagović 45°37ʹ51ʺN, 15°35ʹ27ʺE WL 45 7. Zagreb 45°48ʹ47ʺN, 15°58ʹ40ʺE WL 77 8. Vukmeričke Gorice, Prkovec 45°37ʹ00ʺN, 15°56ʹ59ʺE WL 84 9. Peščenica na Odri 45°36ʹ14ʺN, 16°09ʹ22ʺE WL 95 10. Velebit, Golići 44°42ʹ09ʺN, 15°00ʹ15ʺE WK 04 11. Plitvice, Crna rijeka 44°50ʹ41ʺN, 15°37ʹ45ʺE WK 46 12. Korenica 44°44ʹ37ʺN, 15°42ʹ24ʺE WK 56 13. Učka 45°17ʹ01ʺN, 14°14ʹ58ʺE VL 31 14. Risnjak 45°25ʹ37ʺN, 14°44ʹ45ʺE VL 53 15. Velebit, Zavižan 44°48ʹ09ʺN, 14°58ʹ25ʺE VK 96 16. Velebit, Krivi Put 45°01ʹ56ʺN, 14°57ʹ47ʺE VK 98 17. Kozjak, Malačka 43°34ʹ44ʺN, 16°21ʹ04ʺE XJ 02 half of the last century, the ectoparasitic entomofauna of 2003, 2007, and 2010 in autumn from the period of October mammals was intensively studied by entomologists from to December were sporadic cases of recorded the Slovenian Museum of Natural History in the territory (Tucak et al., 2012). In 2014, one of us (SK) received 12 of the former Yugoslavia (Brelih, 1986; Brelih and Trilar, specimens of lice collected from calves on a small family 2000, 2004). In addition, in these studies, some specimens farm in the village of Vuka (Osječko-baranjska county). of blood sucking lice from different hosts in Croatia were All collected specimens were the long-nosed collected. Summarized data of blood sucking lice fauna of (L. vituli). Within two months, three calves died, possibly Croatia are hard to compare with those of other neighboring as a consequence of infestation with L. vituli that had been countries in the Western and Central Balkans or other present in high numbers on the calves. Heavy infestations European countries, mainly due to sporadic sampling. In with L. vituli are often the cause of anemia and mortality in neighboring Hungary, 43 species of Anoplura classified in calves (Otter et al., 2003). A large number of L. vituli were 7 families were recorded (Vas et al., 2012), while in Turkey also observed on calves in the village of Vuka in September. 20 species were recorded (İnci et al., 2010) from which 12 Lice are often difficult to find on live animals during the species occur in Croatia. To date, in Croatian fauna only summer months, when they are probably present in low 13 species and two subspecies from the suborder Anoplura numbers in refugia; some parts of the body are difficult have been recorded. These data clearly show that the fauna to examine on live animals (Colwell, 2014). In the louse- of blood sucking lice from the suborder Anoplura have infested calves, high frequency of infestation always been poorly studied in Croatia. Similarly, in Italy and in causes significant changes in host behavior, manifested the Republic of Macedonia, Anoplura fauna has also been by persistent rubbing, scratching, and self-licking (Weeks poorly studied (Fois, 2014; Hristovski et al., 2015). Only et al., 1995). Similar behavior was observed in calves 14 species of blood sucking lice were recorded on Sardinia on the farm in the village of Vuka. The present list does and in the territory of the Republic of Macedonia (Fois, not represent a complete report of Croatian Anoplura. 2014; Hristovski et al., 2015). In December 2012, the We can expect to record some species that are known in heads of two pupils from an elementary school, Kneževi neighboring countries, for instance in Hungary. Vinogradi, were infected with 17 specimens of human lice A list of the host species and blood sucking lice (Ped. humanus capitis). Pediculosis was observed only on collected on them nine children in the school. In the territory of Osječko- Class Mammalia baranjska county in the period from 1996 till 2010, only in Order Artiodactyla

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Family Bovidae Family Hominidae Genus Bos Linnaeus, 1758 Genus Homo Linnaeus, 1758 B. taurus Linnaeus 1758 H. sapiens Linnaeus, 1758 Anoplura species: L. vituli, Hae. eurysternus Anoplura species and subspecies: Pth. pubis, Ped. Genus Capra Linnaeus, 1758 humanus capitis, Ped. humanus humanus Ca. hircus (Linnaeus, 1758) The list of Anoplura species and subspecies recorded Anoplura species: L. stenopsis in Croatia Genus Ovis Linnaeus, 1758 For each species and subspecies: sex, locality, month or O. aries Linnaeus, 1758 date, host species, and data source are recorded. Anoplura species: L. pedalis Order Phthiraptera Family Suidae Suborder Anoplura Genus Sus Linnaeus, 1758 Superfamily Linognathoidea S. scrofa Linnaeus, 1758 Family Hoplopleuridae Anoplura species: Hae. apri, Hae. suis Genus Hoplopleura Enderlein, 1904 Order Carnivora Ho. acanthopus (Burmeister, 1839) Family Canidae ♂♂ Risnjak, 8.VIII.1967, from A. sylvaticus, Leg: S. Genus Canis Linnaeus, 1758 Brelih C. lupus Linnaeus, 1758 ♀♀, ♂♂ Plitvice, Crna rijeka, 12.VIII.1968, from M. Anoplura species: L. setosus subterraneus, Leg: S. Brelih C. lupus familiaris Linnaeus, 1758 ♀♀, ♂♂ Učka, 12.VII.1969, from M. subterraneus, Anoplura species: L. setosus Leg: S. Brelih Order Perissodactyla ♀♀ Velebit, Golići, 7.VIII. 1977, from M. liechtensteini, Family Equidae Leg: N. Tvrtković Genus Equus Linnaeus, 1758 ♀♀, ♂♂ Korenica, 20.IX.1987, from Cl. glareolus, Leg: E. asinus Linnaeus, 1758 N. Tvrtković Anoplura species: Hae. asini Ho. affinis (Burmeister, 1839) E. caballus Linnaeus, 1758 ♂♂ Peščenica na Odri, 10.VII.1974, from A. agrarius, Anoplura species: Hae. asini Leg: N. Tvrtković Order Rodentia ♀♀ Vukmeričke Gorice, Prkovec, 19.VII.1974, from A. Family Muridae agrarius, Leg: N. Tvrtković Genus Apodemus Kaup, 1829 ♀♀ Bilje, 12.X.1974, from A. agrarius, Leg: N. Tvrtković A. agrarius (Pallas, 1771) Family Linognathidae Anoplura species: Ho. affinis, P. serrata Genus Linognathus Enderlein, 1905 A. flavicollis (Melchior, 1834) L. pedalis (Osborn, 1896) Anoplura species: P. serrata ♀♀, ♂♂ Zagreb, - VI.1937, from O. aries, (Mikačić, A. mystacinus (Danford et Alston, 1877) 1938) Anoplura species: P. serrata L. setosus (von Olfers, 1816) A. sylvaticus (Linnaeus, 1758) ♀♀, ♂♂ Krivi Put, date unknown, from C. lupus, Anoplura species: Ho. acanthopus, P. serrata (Ferris, 1923, 1951) Genus Clethrionomys Tilesius, 1850 ♀♀, ♂♂ Zagreb, date unknown, from C. lupus Cl. glareolus (Schreber, 1780) familiaris, (Babić, 1934) Anoplura species: Ho. acanthopus L. stenopsis (Burmeister, 1838) Genus Microtus Schrank, 1798 ♀♀, ♂♂ Zagreb, date unknown, from Ca. hircus, M. liechtensteini (Wettstein, 1927) (Babić, 1934) Anoplura species: Ho.acanthopus L. vituli (Linnaeus, 1758) M. subterraneus (de Selys-Longchamps, 1836) ♀♀, ♂♂ Zagreb, 11.X.1937–29.VII.1940, from B. Anoplura species: Ho. acanthopus taurus, (Babić, 1934; Mikačić, 1941) Genus Rattus Fischer, 1803 ♀♀, ♂♂ Vuka, 11.IX.2014, from B. taurus, Leg: S. R. norvegicus (Berkenhout, 1769) Šegović Anoplura species: P. spinu l o s a Family Polyplacidae R. rattus (Linnaeus, 1758) Genus Polyplax Enderlein, 1904 Anoplura species: P. spinu l o s a P. s e r rata (Burmeister, 1839) Order Primates ♀♀ Bilje, 29.IV.1970, from A. agrarius, Leg: G. Džukić

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♀♀, ♂♂ Kozjak, Malačka, 29.IV.1974, from A. ♀♀, ♂♂ Zagreb, date unknown, from E. asinus, (Vražić mystacinus, Leg: S. Brelih and Rijavec, 1960) ♀♀, ♂♂ Risnjak, 8.VIII.1976, from A. sylvaticus, Leg: Hae. eurysternus (Nitzsch, 1818) S. Brelih ♀♀, ♂♂ Zagreb, 11.X.1937–29.VII.1940, from B. ♂♂ Risnjak, 9.VIII.1976, from A. flavicollis, Leg: S. taurus, (Babić, 1934; Mikačić, 1941) Brelih Hae. suis (Linnaeus, 1758) P. spinulosa (Burmeister, 1839) ♀♀, ♂♂ Zagreb, date unknown, S. domesticus, (Babić, ♀♀, ♂♂ Zagreb, date unknown, from R. norvegicus, 1934) (Babić, 1934) ♀♀, ♂♂ Zagreb, 1.XII.1965, from S. scrofa, Leg: J. ♀♀, ♂♂ Velika Kapela, Vrelo, 19.VIII.1968, from R. Dovič rattus, Leg: S. Brelih Family: Pediculidae ♀♀, ♂♂ Otok, Domagović -, II.-VI.2001, from R. Genus Pediculus Linnaeus, 1758 norvegicus, (Stojčević et al., 2004) Ped. humanus capitis (Degeer, 1778) Family Pthiridae ♀♀, ♂♂ Croatia, (Richter, 1982) Genus Pthirus Leach, 1815 ♀♀, ♂♂ Zmajevac, 4. XII. 2012, from H. sapiens, Leg: Pth. pubis (Linnaeus, 1758) ♀♀, ♂♂ Zagreb, date unknown, from H. sapiens, S. Krčmar (Budimčić et al., 2009) Ped. humanus humanus (Linnaeus, 1758) Superfamily Pediculoidea ♀♀, ♂♂ Croatia, (Richter, 1982) Family Haematopinidae Genus Haematopinus Leach, 1815 Acknowledgments Hae. apri Goureau, 1866 We would like to thank Mirjam Lopina (National and ♀♀, ♂♂ Zavižan, 5.VIII.1977, from S. scrofa, Leg: A. University Library in Zagreb) for assistance in collecting Vukušić the literature data. We would also like to thank Savo Hae. asini (Linnaeus, 1758) Brelih, Nikola Tvrtković, Georg Džukić, AnteVukušić, ♀♀, ♂♂ Zagreb, date unknown, from E. caballus, Janez Dovič, and Sanja Šegović for donations of collected (Babić, 1934). material.

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